Investigation of the 2018 thick-billed murre (Uria lomvia) die-off on St. Lawrence Island rules out food shortage as the cause

Abstract

Die-offs of seabirds in Alaska have occurred with increased frequency since 2015. In 2018, on St. Lawrence Island, seabirds were reported washing up dead on beaches starting in late May, peaking in June, and continuing until early August. The cause of death was documented to be starvation, leading to the conclusion that a severe food shortage was to blame. We use physiology and colony-based observations to examine whether food shortage is a sufficient explanation for the die-off, or if evidence indicates an alternative cause of starvation such as disease. Specifically, we address what species were most affected, the timing of possible food shortages, and food shortage severity in a historical context. We found that thick-billed murres (Uria lomvia) were most affected by the die-off, making up 61% of all bird carcasses encountered during beach surveys. Thick-billed murre carcasses were proportionately more numerous (26:1) than would be expected based on ratios of thick-billed murres to co-occurring common murres (U. aalge) observed on breeding study plots (7:1). Concentrations of the stress hormone corticosterone, a reliable physiological indicator of nutritional stress, in thick-billed murre feathers grown in the fall indicate that foraging conditions in the northern Bering Sea were poor in the fall of 2017 and comparable in severity to those experienced by murres during the 1976-1977 Bering Sea regime shift. Concentrations of corticosterone in feathers grown during the pre-breeding molt indicate that foraging conditions in late winter 2018 were similar to previous years. The 2018 murre egg harvest in the village of Savoonga (on St. Lawrence Is.) was one-fifth the 1993-2012 average, and residents observed that fewer birds laid eggs in 2018. Exposure of thick-billed murres to nutritional stress in August, however, was no different in 2018 compared to 2016, 2017, and 2019, and was comparable to levels observed on St. George Island in 2003-2017. Prey abundance, measured by the National Oceanic and Atmospheric Administration in bottom-trawl surveys, was also similar in 2018 to 2017 and 2019, supporting the evidence that food was not scarce in the summer of 2018 in the vicinity of St. Lawrence Island. Of two moribund thick-billed murres collected at the end of the mortality event, one tested positive for a novel re-assortment H10 strain of avian influenza with Eurasian components, likely contracted during the non-breeding season. It is not currently known how widely spread infection of murres with the novel virus was, thus insufficient evidence exists to attribute the die-off to an outbreak of avian influenza. We conclude that food shortage alone is not an adequate explanation for the mortality of thick-billed murres in 2018, and highlight the importance of rapid response to mortality events in order to document alternative or confounding causes of mortality.

Keywords: Arctic; Avian influenza; Feather corticosterone; Food shortage; Marine environment; Mortality; Nutritional stress; Seabirds; Subsistence harvest; Winter.

Figure 1

Beach surveys on St. Lawrence Island were conducted between Kangi and Avighteq, the black triangles indicate these furthest western and eastern extents of our surveys. Colony-based work occurred at Kevipak, Myughi, Tanti and Tuqaghuk (solid circles). The 5 repeated beach transect locations are marked with inverted empty triangles. Study location (middle panel), includes points for the study area bottom-trawl survey stations used in the analysis of prey abundance. Occasionally weak and lethargic thick-billed murres were encountered during surveys (photo credit A. Will). Base map is adapted from Stamen Maps, ©OpenStreetMap contributors, openstreetmap.org/copyright, license CC BY-SA.

Figure 2

Beached bird surveys from 2018 (left) and 2019 (right). 420 bird carcasses were encountered in 2018, 66 carcasses were encountered in 2019. All birds were identified to the level of genus or species, here we show the larid and alcid family (except for murres) for simplification.

Figure 3

Corticosterone concentrations in fall grown primary feathers (left panel) and late-winter grown throat feathers (right panel) sampled from breeding thick-billed murres on St. Lawrence Island compared to historical concentrations from birds collected in the northern Bering Sea region. Fall 2017 and late winter 2018 values include samples from both live birds and beach carcasses. Boxplots indicate the data quartiles centered on the median, raw data are overlain as grey points, bold points are those that are 1.5 * the interquartile range below or above the middle 50% of the data (the value for quartile 1 and 3 respectively). Sample sizes are noted above each boxplot.

Figure 4

Corticosterone concentrations in blood plasma sampled from breeding thick-billed murres on St. George Island in the southeastern Bering Sea (data reproduced here from Kokubun et al., 2018) and on St. Lawrence Island. Boxplots indicate the data quartiles centered on the median, raw data are overlain as grey points, bold points are those that are 1.5 * the interquartile range below or above the middle 50% of the data (the value for quartile 1 and 3 respectively). Sample sizes for this study are noted above each boxplot.

Figure 5

A comparison of exposure to nutritional stress in thick-billed murres that were found dead (n = 32) and alive (n = 7) in the summer of 2018, during (left panel) the fall, when thick-billed murres are in the northern Bering and Chukchi Seas, and (right panel) late winter, when thick-billed murres are likely outside of the ice-covered Pacific Arctic. Boxplots indicate the data quartiles centered on the median, raw data are overlain as grey points, bold points are those that are 1.5 * the interquartile range below or above the middle 50% of the data (the value for quartile 1 and 3 respectively).

Figure 6

Fish abundance as the mean catch per unit effort (CPUE) log-transformed number of individuals and mean CPUE log-transformed biomass in kg/km² for 2017–2019. Bottom-trawl survey results are displayed for the area north of St. Lawrence Island (top), and the greater Northern Bering Sea region (bottom).

Figure 7

Phylogenetic analysis of the H10 (A) and N6 (B) RNA segments using the Neighbor-Joining method. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches. Representative viruses from the Eurasian lineage are denoted with a white circle symbol and from the North American lineage with a black circle symbol. The 2018 murre H10N6 virus is denoted with a red diamond symbol.